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https://doi.org/10.1130/G48333.1
Manuscript received 27 August 2020
Revised manuscript received 26 November 2020
Manuscript accepted 3 December 2020
© 2021 The Authors. Gold Open Access: This paper is published under the terms of the CC-BY license.
Metal-induced stress in survivor plants following
the end-Permian collapse of land ecosystems
Daoliang Chu1*, Jacopo Dal Corso1, Wenchao Shu1, Haijun Song1, Paul B. Wignall2, Stephen E. Grasby3,
Bas van de Schootbrugge4, Keqing Zong5, Yuyang Wu1 and Jinnan Tong1
1
tate Key Laboratory of Biogeology and Environmental Geology, School of Earth Sciences, China University of Geosciences,
S
Wuhan 430074, China
2
School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK
3
Geological Survey of Canada, Natural Resources Canada, Calgary, Alberta T2L2A7, Canada
4
Department of Earth Sciences, Utrecht University, Utrecht 3584 CB, Netherlands
5
School of Earth Sciences, State Key Laboratory of Geological Processes and Mineral Resources, China University of Geosciences,
Wuhan 430074, China
ABSTRACT (e.g., Visscher et al., 2004), but no independent
Teratological spores and pollen are widespread in sediments that record the Permian- evidence has yet been found. Pollution of the
Triassic mass extinction. The malformations are thought to be the result of extreme envi- atmosphere by volcanic volatiles, in particular
ronmental conditions at that time, but the mutagenic agents and the precise timing of the Hg, has been postulated as a possible cause of
events remain unclear. We examined the abundance of teratological sporomorphs and metal malformed plant spores (Hochuli et al., 2017).
concentrations in a Permian-Triassic tropical peatland succession of southwestern China. We Similarly, Lindström et al. (2019) suggested that
find a significant peak of spore tetrads of lycopsid plants (as much as 19% of all sporomorphs) a correlation between teratological sporomorphs
coeval with increases in Cu and Hg concentrations above the main terrestrial extinction and Hg enrichments across the end-Triassic
interval, which marks the loss of Permian Gigantopteris forests, increased wildfire activity, mass extinction indicates mutagenic effects of
and the disappearance of coal beds. Thus, in tropical peatlands, mutagenesis affected only emissions from the Central Atlantic magmatic
surviving plants. Mutagenesis was likely caused by metal toxicity, linked to increased Hg and province. Phytotoxic volcanic gas emissions can
Cu loading, but was not itself a direct cause of the terrestrial crisis. cause abnormalities in plants and their spores
or pollen, including stunted growth, lesions,
INTRODUCTION content of coastal sediments, and frequent malformed spores and pollen, and tetrads (e.g.,
The Permian-Triassic mass extinction wildfires in terrestrial sections of southwestern Lindström et al., 2019).
(PTME) had a catastrophic impact on both ma- China (Chu et al., 2020; Dal Corso et al., 2020). A marked increase of Hg concentrations,
rine and terrestrial ecosystems and was the most Some vegetation survived the collapse of the as well as of other heavy metals like Cu, has
severe crisis of the Phanerozoic (e.g., Wignall, Permian terrestrial ecosystems in the tropics, as been found in many Permian-Triassic bound-
2015). The contemporaneous eruption of the Si- seen in southwestern China, where the luxuriant ary marine and terrestrial successions (Grasby
berian Traps large igneous province is thought Permian Gigantopteris-dominated rainforests et al., 2015, 2019; Shen et al., 2019; Wang et al.,
to have been the main trigger of the biologi- were replaced by herblands comprising almost 2019; Chu et al., 2020). Improved chronology
cal crisis, with the release of vast quantities of monospecific lycophyte populations (Feng et al., of the terrestrial records of the PTME (e.g., Chu
volatiles such as CO2, SO2, organohalogens, and 2020). et al., 2020), where floral changes are better
metals to the atmosphere resulting in the col- Spore tetrads and pollen malformations have documented, allows exploration of the cause-
lapse of the biosphere (Beerling et al., 2007; been observed globally in sediments deposited and-effect relationship between the collapse of
Bond and Wignall, 2014; Burgess et al., 2017; during the PTME and are commonly reported in ecosystems on land, the geochemical changes
Broadley et al., 2018). Work in Australia and relatively high abundances in some quantitative observed, and the occurrence of mutated spores
southwestern China showed that collapse of the studies (e.g., Looy et al., 2001, 2005; Visscher and pollen. Hence, we investigated phytotoxic
terrestrial ecosystems occurred prior to the ma- et al., 2004; Hochuli et al., 2017; Fig. 1). These heavy metal concentrations and stress responses
rine mass extinction (Fielding et al., 2019; Chu malformations have been attributed to the effects of terrestrial plants, specifically in the record
et al., 2020). The loss of terrestrial ecosystems on plants of extreme environmental conditions of spore tetrad abundances, in a well-calibrated
is evidenced by the sudden disappearance of the (Visscher et al., 2004; Foster and Afonin, 2005; terrestrial Permian-Triassic boundary section in
Gigantopteris flora and coal swamps, an abrupt Hochuli et al., 2017; Benca et al., 2018). How- southwestern China.
drop to very low total organic carbon (TOC) ever, no consensus exists on the actual stressor.
Increased levels of ultraviolet-B (UV-B) ra- MATERIALS AND METHODS
diation associated with ozone-layer depletion We studied the ZK4703 borehole from
*E-mail: chudl@cug.edu.cn has been invoked as a possible mutating agent the South China block (drilled 15 km south
CITATION: Chu, D., et al., 2021, Metal-induced stress in survivor plants following the end-Permian collapse of land ecosystems: Geology, v. 49, p. XXX–XXX,
https://doi.org/10.1130/G48333.1
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Figure 1. Paleogeographic transitional Kayitou, and earliest Triassic
map showing locations Dongchuan Formations (Fig. 2). Mudrock
of lycopsid spore tetrad
samples were processed using standard paly-
and metal enrichment
occurrences at the Perm- nological acid maceration techniques involv-
ian-Triassic transition, and ing digestion of 40 g of mudstone in hydro-
location of the ZK4703 chloric and hydrofluoric acid, then dilution
borehole (25.54151°N, with ultrapure water to reach neutral pH.
104.28994°E, present-
day coordinates). (A) The residue was sieved over a 100 μm mesh
Sverdrup Basin, Arctic screen, and both size fractions were collect-
Canada. (B) Hungary. (C) ed. The organic and inorganic residues in the
Italy. (D) Dalongkou, Jung-RESULTS
The palynological and geochemical data are
provided in the Supplemental Material1 and in
Figure 2. Cu concentrations are plotted along
with values normalized to Al, to account for po-
tential lithologic changes, and to TOC, given
that Cu bonds with organic matter in terrestrial
plants and soil. Cu values are relatively constant
from the Xuanwei Formation to the base of the
Kayitou Formation but increase in concentration
(and also Cu/Al and Cu/TOC) above this, reach-
ing a peak Cu value of 417 ppm (Fig. 2D). Hg A B C
and Hg/TOC rise above background levels fol-
lowing the drop in TOC and immediately above
the onset of a negative carbon isotope excursion
(CIE) (Fig. 2; Chu et al., 2020). High Hg con-
centrations are observed in a ∼2 m interval of
the lower part of Kayitou Formation where Hg
increased >10× above background levels (as
high as 324 ppb) (Fig. 2C). Other heavy min-
erals, e.g., Ni, Pb, Cr, and Zn, show very low
concentrations and no changes across the section
(see Table S1 in the Supplemental Material).
Temporal trends of tetrad abundances for
the ZK4703 core were examined by calculat-
ing their frequency in the total number of spores.
Spore tetrads are rare and their frequency never D E
exceed 1% of all spores from the Xuanwei For-
mation to the base of the Kayitou Formation
(Fig. 2E). A distinct peak of tetrads is then ob-
served in the Kayitou Formation where Hg and
Cu enrichments occur. At this level, as much
as 19% of all spores are tetrads (Fig. 2E). The
peak in tetrad abundance is precisely synchro-
nous with the Cu peak (Figs. 2D and 2E). All
the tetrads and normal spores showed the same
taphonomic features and thermal alteration stage
throughout the succession, indicated by the uni-
form phytoclast composition and palynomorph
color (Fig. 3; Fig. S1; Chu et al., 2020), rul-
ing out selective recycling. Tetrads are essen-
tially absent below and above their interval of F G
peak abundance. The lycopsid tetrads belong to
Aratrisporites yunnanensis and Lapposisporites Figure 3. Selection of normal and tetrad spores from sample ZK-41 of ZK4703 borehole,
southwestern China (25.54151°N, 104.28994°E). (A–C) Aratrisporites spp. (normal). (D) Lappo-
echinatus (e.g., Ouyang and Norris, 1999). sisporites echinatus (dyad or one half of tetrad). (E–G) Unseparated tetrads of Lapposisporites
echinatus. Scale bar is 20 μm.
DISCUSSION
In southwestern China, an increase in lycop- In both extant and fossil assemblages, mal- increases in immature tetrads of survivor lyco-
sid tetrads occurred after the collapse of the ter- formed sporomorphs >5% of the total popula- phytes have been found in Greenland and Nor-
restrial ecosystem, which is marked by a sharp tion indicates environmental stress (e.g., Lind- way and have been explained as the possible
decline in TOC to almost 0%; it coincides with ström et al., 1997; Foster and Afonin, 2005), and effect of prolonged UV-B radiation on plants
an interval of increased Cu and Hg concentra- modern studies show that an increased abun- or atmospheric pollution by toxic metals (Viss-
tions and occurs within the negative CIE (Fig. 2). dance of teratologic sporomorphs is an indicator cher et al., 2004; Hochuli et al., 2017). Lycop-
Correlation of the δ13Corg and Hg records indi- of local environmental disturbance (e.g., Mičieta sids were widespread during the PTME interval
cates that the tetrad spike is synchronous with and Murín, 1996). The peak frequencies of tet- and are considered stress-tolerant opportunistic
the marine mass extinction (Chu et al., 2020). rads in our study (6%–19%) therefore indicate plants, capable of surviving the terrestrial catas-
considerable environmental stress. However, the trophe (e.g., Looy et al., 2001; Visscher et al.,
increase in lycopsid tetrads occurs immediately 2004). However, even these hardy plants were
1
Supplemental Material. Description of the studied after the floral extinctions and last coal beds, clearly suffering high levels of stress in the ex-
borehole, analytical methods, supplemental figure, indicating ecological pressure was focused on tinction aftermath.
and data tables. Please visit https://doi.org/10.1130/
GEOL.S.13584935 to access the supplemental mate- the surviving lycopsids. Intriguingly, lycopsids Data normalized for TOC and Al contents
rial, and contact editing@geosociety.org with any do not display this stress indicator at the time show that the Hg and Cu peaks are not due to
questions. of extinction amongst the Permian flora. Similar changes in organic carbon contents nor l ithology
Geological Society of America | GEOLOGY | Volume XX | Number XX | www.gsapubs.org 3
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by guestbut are instead the result of enhanced metal growth inhibition and lipid peroxidation (İşeri Foundation of China (grants 42072025 and 41821001),
loading. To date, a sharp Hg spike has been et al., 2011). We therefore propose that metal and the UK Natural Environment Research Council’s
Eco-PT project (grant NE/P01377224/1), which is a
widely observed in numerous marine PTME genotoxicity most likely caused the observed part of the Biosphere Evolution, Transitions and Resil-
intervals (e.g., Grasby et al., 2015, 2019; Wang malformations in the survivor lycophytes at the ience (BETR) Program.
et al., 2019) as well as in some terrestrial re- PTME, as also invoked for the marine extinction
cords (Shen et al., 2019; Chu et al., 2020). The (Grasby et al., 2015, 2020), but was not observed REFERENCES CITED
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